Al Toufailia H, Scandian L, Shackleton K, Ratnieks FLW (2018) Towards integrated control of varroa: (4) varroa mortality from treating broodless winter colonies twice with oxalic acid via sublimation. J Apic Res 57:438–443. doi: https://doi.org/10.1080/00218839.2018.1454035
Article
Google Scholar
Alizon S, Hurford A, Mideo N, Van Baalen M (2009) Virulence evolution and the trade-off hypothesis: History, current state of affairs and the future. J Evol Biol 22:245–259. doi: https://doi.org/10.1111/j.1420-9101.2008.01658.x
CAS
Article
PubMed
Google Scholar
Amiri E, Strand MK, Rueppell O, Tarpy DR (2017) Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health. Insects 8:48. doi: https://doi.org/10.3390/insects8020048
Article
PubMed Central
Google Scholar
Anderson DL (2000) Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie 31:281–292. doi: https://doi.org/10.1051/apido:2000122
Article
Google Scholar
Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426. doi: https://doi.org/10.1017/S0031182000055360
Article
PubMed
Google Scholar
Antia R, Levin BR, May RM (1994) Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am Nat 144:457–472
Article
Google Scholar
Atkins KE, Read AF, Savill NJ, et al (2013) Vaccination and reduced cohort duration can drive virulence evolution: Marek’s disease virus and industrialized agriculture. Evolution 67:851–860. doi: https://doi.org/10.1111/j.1558-5646.2012.01803.x
CAS
Article
PubMed
Google Scholar
Best A, White A, Boots M (2009) The implications of coevolutionary dynamics to host-parasite interactions. Am Nat 173:779–791. doi: https://doi.org/10.1086/593132
Article
PubMed
Google Scholar
Boecking O, Genersch E (2008) Varroosis – the Ongoing Crisis in Bee Keeping. Journal für Verbraucherschutz und Lebensmittelsicherheit 3(2):221–228
Boots M, Mealor M (2007) Local interactions select for lower pathogen infectivity. Science 315:1284–1286. doi: https://doi.org/10.1126/science.1137126
CAS
Article
PubMed
Google Scholar
Boots M, Sasaki A (1999) ‘Small worlds’ and the evolution of virulence: Infection occurs locally and at a distance. Proc R Soc Lond B Biol Sci 266:1933–1938
CAS
Article
Google Scholar
Boots M, Hudson PJ, Sasaki A (2004) Large shifts in pathogen virulence relate to host population structure. Science 303:842–844
CAS
Article
Google Scholar
Branco MR, Kidd NAC, Pickard RS (2006) A comparative evaluation of sampling methods for Varroa destructor (Acari: Varroidae) population estimation. Apidologie 37:452–461. doi: https://doi.org/10.1051/apido:2006010
Article
Google Scholar
Bremermann HJ, Pickering J (1983) A game-theoretical model of parasite virulence. J Theor Biol 100:411–426. doi: https://doi.org/10.1016/0022-5193(83)90438-1
CAS
Article
PubMed
Google Scholar
Brosi BJ, Delaplane KS, Boots M, de Roode JC (2017) Ecological and evolutionary approaches to managing honeybee disease. Nat Ecol Evol 1:1250–1262. doi: https://doi.org/10.1038/s41559-017-0246-z
Article
PubMed
PubMed Central
Google Scholar
Bull JJ (1994) Virulence. Evolution 48:1423–1437. doi: https://doi.org/10.2307/2410237
CAS
Article
PubMed
Google Scholar
Calderón R, van Veen J, Sommeijer M, Sanchez L (2010) Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp Appl Acarol 50:281–297. doi: https://doi.org/10.1007/s10493-009-9325-4
Article
PubMed
Google Scholar
Carius HJ, Little TJ, Ebert D (2001) Genetic variation in a host-parasite association: Potential for coevolution and frequency-dependent selection. Evolution 55:1136–1145. doi: https://doi.org/10.1111/j.0014-3820.2001.tb00633.x
CAS
Article
PubMed
Google Scholar
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Google Scholar
Corrêa-Marques MH, De Jong D, Rosenkranz P, Gonçalves LS (2002) Varroa-tolerant Italian honey bees introduced from Brazil were not more efficient in defending themselves against the mite Varroa destructor than Carniolan bees in Germany. Genet Mol Res 1:153–158
PubMed
Google Scholar
Corrêa-Marques MH, Medina LM, Martin SJ, De Jong D (2003) Comparing data on the reproduction of Varroa destructor. Genet Mol Res 2:1–6
PubMed
Google Scholar
Dahle B (2010) The role of Varroa destructor for honey bee colony losses in Norway. J Apic Res 49:124–125
Article
Google Scholar
De Jong D, Soares A (1997) An isolated population of Italian bees that has survived Varroa jacobsoni infestation without treatment for over 12 years. Am Bee J 137
De Roode JC, Altizer S (2010) Host–parasite genetic interactions and virulence-transmission relationships in natural populations of monarch butterflies. Evolution 64:502–514. doi: https://doi.org/10.1111/j.1558-5646.2009.00845.x
Article
PubMed
Google Scholar
De Roode JC, Yates AJ, Altizer S (2008) Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc Natl Acad Sci 105:7489–7494. doi: https://doi.org/10.1073/pnas.0710909105
Article
PubMed
Google Scholar
Delaplane KS, Hood WM (1999) Economic threshold for Varroa jacobsoni Oud. in the southeastern USA. Ap 30:383–395
Google Scholar
Delaplane KS, van der Steen J, Guzman-Novoa E (2013) Standard methods for estimating strength parameters of Apis mellifera colonies. J Apic Res 52:1–12. doi: https://doi.org/10.3896/IBRA.1.52.1.03
Article
Google Scholar
Dodge Y, Cox D, Commenges D, et al (eds) (2006) The Oxford Dictionary of Statistical Terms, 6th. Oxford University Press, Oxford
Google Scholar
Dynes T, de Roode JC, Lyons JI, et al (2017) Fine scale population genetic structure of Varroa destructor, an ectoparasitic mite of the honey bee (Apis mellifera). Parasitology 48:93–101. doi: https://doi.org/10.1007/s13592-016-0453-7
Article
Google Scholar
Dynes TL, Berry JA, Delaplane KS, et al (2019) Reduced density and visually complex apiaries reduce parasite load and promote honey production and overwintering survival in honey bees. PLOS ONE 14:e0216286. doi: https://doi.org/10.1371/journal.pone.0216286
CAS
Article
PubMed
PubMed Central
Google Scholar
Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 14:465–485
Article
Google Scholar
Fries I, Camazine S (2001) Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32:199–214. doi: https://doi.org/10.1051/apido:2001122
Article
Google Scholar
Fries I, Aarhus A, Hansen H, Korpela S (1991) Comparison of diagnostic methods for detection of low infestation levels of Varroa jacobsoni in honey-bee (Apis mellifera) colonies. Exp Appl Acarol 10:279–287. doi: https://doi.org/10.1007/BF01198656
Article
Google Scholar
Gibson, Stoy K. S., Gelarden I. A., et al (2015) The evolution of reduced antagonism—A role for host–parasite coevolution. Evolution 69:2820–2830. doi: https://doi.org/10.1111/evo.12785
CAS
Article
PubMed
PubMed Central
Google Scholar
Greischar MA, Koskella B (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10:418–434. doi: https://doi.org/10.1111/j.1461-0248.2007.01028.x
Article
PubMed
Google Scholar
Guzmán-Novoa E, Eccles L, Calvete Y, et al (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41:443–450. doi: https://doi.org/10.1051/apido/2009076
Article
Google Scholar
Hawley DM, Osnas EE, Dobson AP, et al (2013) Parallel patterns of increased virulence in a recently emerged wildlife pathogen. PLoS Biol 11:e1001570. doi: https://doi.org/10.1371/journal.pbio.1001570
CAS
Article
PubMed
PubMed Central
Google Scholar
Højsgaard S, Halekoh U, Yan J (2006) The R Package geepack for Generalized Estimating Equations. J Stat Softw 15:1–11. doi: https://doi.org/10.18637/jss.v015.i02
Article
Google Scholar
Hubbard AE, Ahern J, Fleischer NL, et al (2010) To GEE or not to GEE: Comparing population average and mixed models for estimating the associations between neighborhood risk factors and health. Epidemiology 21
Jensen KH, Little T, Skorping A, Ebert D (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4:e197. doi: https://doi.org/10.1371/journal.pbio.0040197
CAS
Article
PubMed
PubMed Central
Google Scholar
Josse J, Husson F (2016) missMDA: A package for handling missing values in multivariate data analysis. J Stat Softw 70:1–31
Article
Google Scholar
Kamo M, Boots M (2006) The evolution of parasite dispersal, transmission, and virulence in spatial host populations. Evol Ecol Res 8:1333–1347
Google Scholar
Kennedy DA, Kurath G, Brito IL, et al (2015) Potential drivers of virulence evolution in aquaculture. Evol Appl 9:344–354. doi: https://doi.org/10.1111/eva.12342
Article
Google Scholar
Kerr B, Neuhauser C, Bohannan BJM, Dean AM (2006) Local migration promotes competitive restraint in a host–pathogen “tragedy of the commons.” Nature 442:75–78. doi: https://doi.org/10.1038/nature04864
CAS
Article
PubMed
Google Scholar
Lambrechts L, Fellous S, Koella JC (2006) Coevolutionary interactions between host and parasite genotypes. Trends Parasitol 22:12–16. doi: https://doi.org/10.1016/j.pt.2005.11.008
Article
PubMed
Google Scholar
Lenski RE, May RM (1994) The evolution of virulence in parasites and pathogens: Reconciliation between two competing hypotheses. J Theor Biol 169:253–265. doi: https://doi.org/10.1006/jtbi.1994.1146
CAS
Article
PubMed
Google Scholar
Lenth RV (2016) Least-squares means: The R Package lsmeans. J Stat Softw 69:1–33
Article
Google Scholar
Levin B (1996) The evolution and maintenance of virulence in microparasites. Emerg Infect Dis 2:93–102. doi: https://doi.org/10.3201/eid0202.960203
CAS
Article
PubMed
PubMed Central
Google Scholar
Levin S, Pimentel D (1981) Selection of intermediate rates of increase in parasite-host systems. Am Nat 117:308–315. doi: https://doi.org/10.2307/2460529
Article
Google Scholar
Lion S, Boots M (2010) Are parasites ‘“prudent”’ in space? Ecol Lett 13:1245–1255. doi: https://doi.org/10.1111/j.1461-0248.2010.01516.x
Article
PubMed
PubMed Central
Google Scholar
Mackinnon MJ, Read AF (1999) Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53:689–703. doi: https://doi.org/10.2307/2640710
Article
PubMed
Google Scholar
Mackinnon MJ, Read AF (2004) Virulence in malaria: An evolutionary viewpoint. Philos Trans R Soc Lond B Biol Sci 359:965–986. doi: https://doi.org/10.1098/rstb.2003.1414
Article
PubMed
PubMed Central
Google Scholar
McMahon DP, Natsopoulou ME, Doublet V, et al (2016) Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc R Soc B Biol Sci 283:. doi: https://doi.org/10.1098/rspb.2016.0811
Messenger SL, Molineux IJ, Bull JJ (1999) Virulence evolution in a virus obeys a trade off. Proc R Soc Lond B Biol Sci 266:397–404. doi: https://doi.org/10.1098/rspb.1999.0651
CAS
Article
Google Scholar
Milani N (2001) Activity of oxalic and citric acids on the mite Varroa destructor in laboratory assays. Apidologie 32:127–138
CAS
Article
Google Scholar
Miller MR, White A, Boots M (2007) The evolution of parasites in response to tolerance in their hosts: The good, the bad, and apparent commensalism. Evolution 60:945–956. doi: https://doi.org/10.1111/j.0014-3820.2006.tb01173.x
Article
Google Scholar
National Research Council (2007) Status of pollinators in North America. The National Academies Press, Washington
Google Scholar
Nolan MP, Delaplane KS (2017) Distance between honey bee Apis mellifera colonies regulates populations of Varroa destructor at a landscape scale. Apidologie 48:8–16. doi: https://doi.org/10.1007/s13592-016-0443-9
Article
Google Scholar
Pettis JS, Delaplane KS (2010) Coordinated responses to honey bee decline in the USA. Apidologie 41:256–263. doi: https://doi.org/10.1051/apido/2010013
Article
Google Scholar
Potts SG, Ngo HT, Biesmeijer JC, et al (2016) The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production
Read AF, Graham AL, Råberg L (2008) Animal defenses against infectious agents: Is damage control more important than pathogen control. PLOS Biol 6:e1000004. doi: https://doi.org/10.1371/journal.pbio.1000004
CAS
Article
Google Scholar
Read AF, Baigent SJ, Powers C, et al (2015) Imperfect vaccination can enhance the transmission of highly virulent pathogens. PLOS Biol 13:e1002198. doi: https://doi.org/10.1371/journal.pbio.1002198
CAS
Article
PubMed
PubMed Central
Google Scholar
Restif O, Koella JC (2003) Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am Nat 161:827–836. doi: https://doi.org/10.1086/375171
Article
PubMed
Google Scholar
Rondeau V, Mazroui Y, Gonzalez JR (2012) frailtypack: An R package for the analysis of correlated survival data with frailty models using penalized likelihood estimation or parametrical estimation. J Stat Softw 47:1–28
Article
Google Scholar
Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103, Supplement:S96–S119. doi: https://doi.org/10.1016/j.jip.2009.07.016
Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: Life history, implications, and impact. Annu Rev Entomol 45:519–548. doi: https://doi.org/10.1146/annurev.ento.45.1.519
CAS
Article
PubMed
Google Scholar
Seeley T (2007) Honey bees of the Arnot Forest: A population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38:19–29. doi: https://doi.org/10.1051/apido:2006055
Article
Google Scholar
Seeley TD, Smith ML (2015) Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie 46:716–727. doi: https://doi.org/10.1007/s13592-015-0361-2
Article
Google Scholar
Vojvodic S, Jensen AB, Markussen B, et al (2011) Genetic variation in virulence among chalkbrood strains infecting honeybees. PLOS ONE 6:e25035. doi: https://doi.org/10.1371/journal.pone.0025035
CAS
Article
PubMed
PubMed Central
Google Scholar
Webb SD, Keeling MJ, Boots M (2013) A theoretical study of the role of spatial population structure in the evolution of parasite virulence. Theor Popul Biol 84:36–45. doi: https://doi.org/10.1016/j.tpb.2012.11.008
Article
PubMed
Google Scholar
Wegener J, Ruhnke H, Scheller K, Mispagel S, Knollmann U, Kamp G, Bienefeld K (2016) Pathogenesis of varroosis at the level of the honey bee (Apis mellifera) colony. Journal of Insect Physiology 91-92:1–9